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First published online October 26, 2007
doi: 10.1242/10.1242/dev.005934
Meeting Review |
Sprott Center for Stem Cell Research, Ottawa Health Research Institute, 501 Smyth Road, Ottawa, ON K1H 8L6, Canada.
* Author for correspondence (e-mail: mrudnicki{at}ohri.ca)
SUMMARY
The FASEB summer research conference on Skeletal Muscle Satellite and Stem Cells, organized by Thomas Rando, Giulio Cossu and Jeffrey Chamberlain, was held in Indian Wells, California, in July. An international array of researchers gathered to share numerous new insights into the cellular and molecular regulation of stem cells and satellite cells in skeletal muscle biology. The conference is unique in that it brings together investigators from diverse backgrounds, who work on the growth and repair of skeletal muscle in humans and model systems, in health and disease.
Introduction
It is now over 45 years since the first description of the canonical
satellite cell in adult skeletal muscle
(Mauro, 1961
). Satellite cells
reside in a niche that lies beneath the basal lamina but outside of the
associated muscle fibers (Fig.
1A) (Bischoff,
1990). Satellite cells have long been believed to represent a
committed muscle progenitor that is responsible for the postnatal growth and
regenerative capacity of skeletal muscle
(Seale et al., 2000).
Typically mitotically quiescent, satellite cells are activated in response to
stress that is induced by weight bearing or by trauma, such as injury
(Charge and Rudnicki, 2004).
The descendants of activated satellite cells, called myogenic precursor cells
or skeletal myoblasts, undergo multiple rounds of division prior to terminal
differentiation and fusion to form multinucleated myofibers.
|
). In
fact, it has been demonstrated recently that satellite cells represent a
heterogeneous, hierarchical population that is composed of a small number of
satellite stem cells and a larger number of committed myogenic progenitors
(Kuang et al., 2007).
Moreover, our understanding of non-conventional myogenic stem cells (side
population cells, mesoangioblasts, and muscle-derived stem cells) has been
clarified by the appreciation that they might be derived from a pericyte-like
cell in muscle tissue (Peault et al.,
2007). These and other advances in our understanding of skeletal
muscle satellite and stem cell biology were discussed at the recent FASEB
conference, which we review below. Developmental origin of satellite cells
From studies performed in chick and mouse, it has been recently suggested
that during early embryogenesis, a cell population that expresses the
paired-box transcription factors Pax3 and Pax7, but not any of the known
skeletal-muscle-specific markers, arises from the medial part of the somitic
dermomyotome. These cells are maintained as a proliferating population
throughout development and then adopt a satellite cell position that is
characteristic of progenitor cells in postnatal muscle
(Fig. 1B)
(Buckingham and Relaix, 2007).
Simon Hughes (King's College, London, UK) discussed the advantages of the
zebrafish model for the study of embryonic myogenesis. Zebrafish embryos are
optically clear, which allows for easy lineage-tracking in live embryos. By
using confocal imaging and informatics systems, researchers can follow the
cellular trajectories of one to hundreds of cells in live zebrafish embryos,
with the ultimate goal of understanding the exact pathways of cellular
movements during embryonic development
(Forouhar et al., 2006).
Furthermore, `external cells' that express Pax3 and Pax7 were recently
identified at the surface of the somite. The analysis of these cells, which
form a dermomyotome-like tissue and give rise to muscle fiber and myoblasts,
should bring new insights into muscle morphogenesis and development in the
near future (Devoto et al.,
2006).
These satellite cell precursors depend on Pax3 and Pax7 expression during
embryogenesis for their commitment into the satellite cell lineage and their
survival, but little is known about the importance of the myogenic regulatory
factors (MRFs), such as MyoD (Myod1, myogenic differentiation 1), Myf5
(myogenic factor 5), Mrf4 (also known as Myf6, myogenic factor 6) and
myogenin, in this lineage. David Goldhamer (University of Connecticut, Storrs,
CT) reported preliminary results obtained with the Cre/loxP
lineage-tracing system in mice. They crossed the reporter strain R26R-EYFP
[which constitutively expresses the yellow fluorescent protein (YFP) reporter
in all cells that undergo recombination at loxP sites] with a new
MyoD-Cre knock-in mouse in which Cre recombinase is expressed under the same
regulatory control as MyoD. Goldhamer's findings lead him to conclude that
most, if not all, satellite cells express MyoD in their developmental history.
By contrast, by crossing a Myf5-Cre line with the R26R-YFP line, Kuang et al.
have found that, after birth, 90% of satellite cells express Myf5 and that
Myf5-negative cells are the repopulating stem cells within the satellite cell
lineage (Kuang et al., 2007).
The differences between the findings of these two studies might be explained
by the use of different markers to identify satellite cells. Future studies
will settle this issue.
It is a common hypothesis that satellite cells are the cells of origin of rhabdomyosarcomas (an aggressive childhood and adult cancer). Charles Keller (University of Texas, San Antonio, TX) used conditional genetics to temporally and spatially restrict the activation of oncogenes or the inactivation of tumor suppressors to subsets of embryonic and postnatal muscle cell precursors in mice. He presented new and exciting experiments in which his team compared the cancerous outcomes of oncogenic recombinations driven within the different expression domains of myogenic genes. Keller's work increasingly links dysregulation of satellite cell development with rhabdomyosarcomas. We believe that such analyses of muscle-related cancers will open new avenues of research in satellite cell biology.
Signaling pathways in satellite cell activation and differentiation
Embryonic and adult myogenesis are closely related; once satellite cells
are activated by a stress to the fiber, they enter the cell cycle and
recapitulate the molecular pathways that occur during the development of the
skeletal muscle, such as the Wnt, Notch and myostatin pathways, which are
crucial regulators of embryonic myogenesis
(Shi and Garry, 2006). All of
these pathways are required for the self-renewal or differentiation of stem
cell progeny in various systems and are believed to be regulators of satellite
cell biology, as discussed in more detail in the following section.
Wnt signaling
After injury, transcripts of the Wnt morphogens, their Frizzled receptors,
and the Wnt antagonists Sfrp (secreted frizzled-related proteins), are
detected in the regenerating skeletal muscle tissue
(Polesskaya et al., 2003), but
a specific role for the Wnt pathway in satellite cell regulation has still not
been described. Thomas Rando's team (Stanford University School of Medicine,
Stanford, CA) have been involved in deciphering the mechanisms that lead to
impaired muscle regeneration with age. He presented new work that demonstrates
that the loss of myogenic phenotype during aging in mice is linked with
elevated Wnt signaling. By using the Pax7-Cre-ER lineage-tracing system, they
found that cells that constitutively express lacZ after
Cre/loxP recombination that once were Pax7-positive satellite cells
can lose Pax7 expression and differentiate into fibroblasts in old muscle. By
contrast, inhibition of Wnt signaling by either Sfrp3 or dickkopf 1 (potent
inhibitors of Wnt canonical signaling), rescues muscle regeneration in aged
mice (Brack et al., 2007).
Peter Zammit (King's College, London, UK) retrovirally infected satellite
cells with constitutively activated forms of ß-catenin and showed that
repression of differentiation and maintenance of Pax7 expression occur in
infected satellite cells, suggesting that forced canonical Wnt signaling is
pro-self-renewal. On the non-canonical side of the story, Charlotte Peterson
(University of Kentucky, Lexington, KY) presented new insights from their
studies of Wnt10b-null mice
(Vertino et al., 2005). The
mutant myoblasts derived from these mice show increased myogenic
differentiation owing to a compensatory increase in Wnt7b, which Peterson
links to the activation of a non-canonical Wnt pathway that potentially
involves Creb proteins. These results appear to be the starting point of a new
and very complex story.
Notch signaling
Notch signaling is potentially a major pathway that regulates the
activation and expansion of the satellite cell lineage during embryogenesis
(Vasyutina et al., 2007) and
in the adult (Conboy and Rando,
2002). The decline of Notch signaling with age is thought to be
another cause of the decreased regenerative potential of aged satellite cells
(Conboy et al., 2005). Reshma
Taneja (Mount Sinai School of Medicine, New York, NY) presented recently
published work that demonstrates that the bHLH transcription factor Stra13
(stimulated by retinoic acid 13) antagonizes Notch1 signaling in mouse
satellite cells and regulates the balance between proliferation and
differentiation during regeneration (Sun
et al., 2007). Addolorata Pisconti from Brad Olwin's lab
(University of Colorado, Boulder, CO) described syndecan 3 (Sdc3) as a new
regulator of Notch signaling. The loss of Sdc3 in mice induces premature
progenitor cell commitment and differentiation. Further description of the
role of Sdc3 in the Notch pathway will be of great interest.
Myostatin
Myostatin belongs to the Tgfß (transforming growth factor ß)
family of secreted molecules and potentially antagonizes muscle regeneration
by limiting satellite cell proliferation and differentiation. Victoria Siriett
and Ravi Kambadur (AgResearch, University of Waikato, Hamilton, New Zealand)
described the use of a myostatin antagonist, Mstn-ant1, for the rescue in
vitro and in vivo of the myostatin inhibitory effect on myogenesis in mice.
Mstn-ant1 delivery was suggested to increase the number of activated satellite
cells and to enhance their migratory potential, as well as regulating Pax7
expression (Siriett et al.,
2007). Thus, antagonism of myostatin appears to represent a
potential therapeutic strategy for aged-induced sarcopenia (the degenerative
loss of skeletal muscle mass and strength in senescence).
Interactions between satellite cells and their microenvironment
The cell migration and chemosensing of myogenic precursors are required for
efficient muscle regeneration, and numerous groups are currently investigating
how satellite cell activation and differentiation are modulated by their
direct microenvironment, either by cell-surface contact or by other
cell-secreted molecules (Chazaud et al.,
2003).
An important effector of myogenic differentiation is the cell-surface
protein Cdo (Cdo1, cysteine dioxygenase 1). Robert Krauss (Mount Sinai School
of Medicine, New York, NY) summarized some of his lab's accomplishments in
characterizing Cdo functions, expression profiles and partners. He presented
exciting new data on Cdo activation and proposed that Cdo works via Bnip2 and
Cdc42 to initiate a signaling cascade that activates the p38 MAP kinase bound
to the scaffold protein JLP (JNK-associated leucine-zipper protein, Spag9)
(Takaesu et al., 2006).
Helen Blau (Stanford University, Stanford, CA) presented exciting new work using engineered scaffolds in artificial niches in vitro to culture stem cells. Blau showed us impressive recordings of time-lapse microscopy of live single cells in hydrogel microwells. It was evident that this approach holds much promise to address experimentally the role of extrinsic tethered and soluble factors that regulate satellite cell fate determination and self-renewal.
Transcription factor control of satellite cell proliferation and differentiation
A handful of specific transcription factors are necessary to drive the
molecular regulation of satellite cells. Daniel Garry (University of
Minnesota, Minneapolis, MN) discussed the molecular regulation of
Foxk1, a member of the forkhead/winged-helix family of transcription
factors. Foxk1-null mice have fewer satellite cells and impaired
regeneration. Foxk1 has recently been described as regulated by Sox15 (SRY-box
containing gene 15) via Fhl3 (four and a half LIM domains 3); all three
transcription factors coordinately regulate the myogenic progenitor cell
population and skeletal muscle regeneration
(Meeson et al., 2007). Garry
presented new results that link the lack of Foxk1 to an induction of p21 in
Foxk1-null cells and discussed a novel pathway in which the Foxk1
repression of p21 results in satellite cell activation.
Pax7 is a major regulator of satellite cell development and differentiation
during embryogenesis and postnatal life. Pax7-null mice show marked
muscle wasting together with a complete absence of functional satellite cells
(Kuang et al., 2006). Michael
Rudnicki (Ottawa Health Research Institute, Ottawa, Canada) presented new
findings on its multiple functions. Genome-wide analysis of Pax7 DNA-binding
sites by chromatin immunoprecipitation (ChIP) combined with high-throughput
sequencing identified candidate Pax7 target genes and implicated Pax7 in
transcriptional networks that are related to many aspects of myogenesis.
Tandem affinity purification and mass spectrometry identified the association
of Pax7 with a histone-methyltransferase complex that leads to the
transcriptional activation of specific chromatin domains. These results lead
to the idea that Pax7 drives the myogenic identity of the satellite cell
lineage through epigenetic modifications.
A novel paradigm for the regulation of Pax7's paralog, Pax3, was described
by Stéphane Boutet from Thomas Rando's lab (Stanford University School
of Medicine, Stanford, CA). He showed that Pax3 is regulated by ubiquitination
and proteasomal degradation during satellite cell activation. Intriguingly, it
is a monoubiquitylated form of Pax3 that undergoes proteasomal degradation and
not a polyubiquitylated form. He showed that specific lysines account for this
regulation and demonstrated that a stable mutant form of Pax3 inhibits
myogenic differentiation. Thus, Boutet proposed that control of Pax3
degradation is an essential step for the progression of the myogenic program
beyond commitment and that monoubiquitylation can also be interpreted as a
destruction signal by the proteasome
(Boutet et al., 2007).
The first targeted mutations of the Myf5/Mrf4 locus in
the early 90's showed that the loss of these genes in mice leads to defects in
primary myotome formation, resulting in severe malformations and in perinatal
death (Braun et al., 1992).
However, the field had to wait for the further characterization of this locus
and for advances in gene targeting before the first viable Myf5-null
mice became available (Kaul et al.,
2000). Both Shahragim Tajbakhsh (Institut Pasteur and CNRS, Paris,
France) and Thomas Braun (Max-Planck Institute for Heart and Lung Research,
Bad Nauheim, Germany) discussed the phenotype of adult Myf5-null
mice. Tajbakhsh reported that mutant mice show signs of repeated regeneration
and more adipose infiltration in the muscle tissue following a freeze injury
(Gayraud-Morel, 2007). Braun
spoke about his recently published work that shows that Myf5 supports
efficient regeneration by enabling transient myoblast regeneration
(Ustanina et al., 2007). They
agreed on the fact that compound Myf5-null/mdx mutants show
constant regeneration and an aggravation of the dystrophic phenotype,
presumably owing to satellite cells lacking proliferative potential
(mdx mice lack functional dystrophin and are thus an animal model of
human Duchenne muscular dystrophy). It is striking, however, that although
Myf5 and MyoD can each compensate for the loss of the other during
embryogenesis, they cannot efficiently compensate for each other in an adult
context, and it is clear that whereas MyoD regulates satellite cell
differentiation, Myf5 function is related to satellite cell proliferation.
Why, and how, the balance between these two MRFs is orchestrated during muscle
regeneration remains elusive; this question will certainly be assessed in the
future.
Satellite cell heterogeneity and self-renewal
Satellite cells directly isolated from adult muscle tissues and grafted
into host mice contribute both to fiber repair and to the muscle satellite
cell compartment (Montarras et al.,
2005). Not all satellite cells possess equal potential within the
lineage; Pax7-positive/Myf-negative satellite cells represent a stem cell
compartment that, following intramuscular transplantation, can extensively
contribute to the satellite cell reservoir throughout a host muscle
(Fig. 1C)
(Kuang et al., 2007).
Numerous researchers are currently trying to find out which satellite cell
population harbors the most potent regenerative and self-renewal potential.
Another important question derives from the observation that the expansion of
satellite cells in culture before their engraftment reduces their regenerative
capacity (Montarras et al.,
2005). What are the differences between quiescent and activated
satellite cells that restrict their stem cell characteristics?
Bradley Olwin (University of Colorado, Boulder, CO) assessed the problem
using BaCl2 to induce in vivo muscle regeneration in mice, followed
by the transplantation of heterologous GFP-positive muscle fibers, without
irradiation or immunosuppression. He described an impressive 
50% increase
in the mass of the recipient muscle 30-60 days after transplantation, proving
that satellite cells' regenerative potential is enhanced by its
microenvironment, the muscle fiber. He also detailed serial transplantation
experiments, in which chimeric fibers extracted from the first grafted muscle
were transplanted into a secondary recipient, and he showed that GFP-positive
satellite cells deriving from the first donor were again able to engraft the
satellite cell pool in the secondary host. The questions arising from this
work include: why does the mass of the grafted muscle increase dramatically
after transplantation? And how do donor cells escape immune surveillance by
the host? If Olwin and his team succeed in answering these questions, they
might represent one of the next major outcomes in our field.
Using a FACS strategy with a selection based on ß1-integrin and Cxcr4 immunoreactivity, which marks 80% of satellite cells, Amy Wagers (Harvard Medical School, Boston, MA) grafted GFP-positive satellite cells into recipient mdx muscle and showed a robust regeneration and restoration of muscle function. She also presented results demonstrating the self-renewal of satellite cells after serial transplantations: GFP-positive satellite cells grafted into a host muscle were purified again after the regeneration of the transplanted tissue and were able to give rise to myogenic colonies in vitro. In the same way, the re-injury of previously engrafted muscle increased the number of GFP-positive cells, suggesting that a de novo recruitment of engrafted cells participates in muscle regeneration.
Terrence Partridge (Children's National Medical Center, Washington, DC),
whose lab first grafted intact myofibers into an adult muscle and proved that
satellite cells self-renew in vivo (Collins
et al., 2005), discussed the difference in grafting efficiency
between satellite cells isolated from different muscles. He also described
differences between satellite cells from young and aged muscle. As grafts of
young and old fibers into host young muscle yield similar reconstruction,
Partridge stated that there is a population of self-replacing satellite cells
within both young and old muscle (Collins
et al., 2007). Hence, the concept that muscle satellite stem cells
survive with age preferentially in comparison to committed cells was supported
by results from Zipora Yablonka-Reuveni's research team (University of
Washington, Seattle, WA). In this group's studies, Myf5 expression was
determined by tracing Myf5-driven reporter activity using the
Myf5-lacZ knock-in mouse. Satellite cells that display Myf5
activity account for 80-90% of the Pax7-positive cells in adult mice. This
proportion goes down to 50% in 2-year-old animals.
Analysis of satellite cell quiescence
Since the cells that repopulate the muscle satellite niche are the ones
that turn off the expression of MyoD and return to a quiescent state
(Olguin and Olwin, 2004;
Zammit et al., 2004), one way
to find new insights into satellite cell self-renewal is to analyze the
molecular regulation of stem cell quiescence. With this question in mind, a
few groups presented their results of global gene analyses of freshly isolated
satellite cells.
Shin'ichi Takeda (National Center of Neurology and Psychiatry, Tokyo,
Japan) discussed the results obtained after microarray analysis of satellite
cells sorted with the SM/C-2.6 antibody (this antibody binds an unknown
antigen that is expressed by most satellite cells)
(Fukada et al., 2007). He
presented new data that suggest that the calcitonin receptor is a potential
new effector of satellite cell quiescence. Calcitonin signaling prevents
satellite cells from entering the cell cycle and inhibits the motility of
primary myoblasts. Takeda also showed that satellite cells lose calcitonin
receptor expression during activation and that a fraction of activated cells
can co-express Pax7 and the calcitonin receptor 7 days after cardiotoxin
injection, corresponding to a return to quiescence.
The Rudnicki lab's strategy for sorting satellite cells with
7-integrin-positive selection and negative selection of CD31 (Pecam1),
Sca1 (Ly6a), CD45 (Ptprc) and CD11b (Itgam), applied to cells extracted from
Myf5-Cre*R26R-YFP mice, allows for the efficient isolation of
satellite progenitor (Myf5-positive) and stem (Myf5-negative) cells. Fabien Le
Grand, from the Rudnicki group, presented results from the comparison of these
populations by subtractive suppressive hybridization. This approach showed
that both satellite progenitor cells and stem cells express specific genes,
and that the hierarchy that exists among these cells is regulated by specific
transcription factors and by the Notch signaling pathway.
Didier Montarras (Institut Pasteur and CNRS, Paris, France) reported
results from a microarray analysis of Pax3-GFP-positive cells extracted from
resting and injured muscle. He identified a large number of transcripts that
are differentially expressed between the two conditions. Interestingly,
Montarras detected genes related to myogenic differentiation in the quiescent
cells and postulated that a fraction of the quiescent cells is always
committed to differentiation (Montarras et
al., 2005).
Some striking comparisons between the different gene expression analyses performed by these three teams were discussed, and a consensus emerged that genes that function in cell cycle arrest, in Notch signaling, and that encode Krüppel-like factors, are strongly expressed by quiescent cells. This area will clearly be the subject of much further research.
Cellular therapies in muscle disease and atrophy
As previously discussed, freshly prepared satellite cells can participate
in skeletal muscle regeneration, but the impossibility of delivering these
cells to patients intravascularly limits their efficiency. Exciting advances
in both cell-mediated and gene-mediated therapies were discussed at this
conference. Giulio Cossu (Hospital San Raffaele, Milan, Italy) presented
results obtained with the adult mesoangioblast, a vessel-derived stem cell
that can be efficiently transplanted by intra-arterial delivery. The latest
advances using these cells resulted in a remarkable clinical amelioration and
preservation of motility in the golden retriever dog model of Duchenne
muscular dystrophy (Sampaolesi et al.,
2006). Cossu also discussed the initiation of the first clinical
trials in humans. Mesoangioblasts will be injected into a small muscle of the
hand of 14- to 16-year-old boys with Duchenne muscular dystrophy. The major
issues for muscle stem cell transplantation in the context of Duchenne
muscular dystrophy remain that the patient must follow an immunosuppressive
treatment and that the transplanted stem cells do not home to the heart, which
is also affected by the lack of dystrophin.
Jeff Chamberlain (University of Washington, Seattle, WA) discussed the use
of viral vectors to stably transduce myogenic stem cells with therapeutic
genes (Li et al., 2006).
Direct intramuscular injection of lentiviral vectors, carrying a
mini-dystrophin-eGFP fusion transgene, into neonatal mdx mice leads
to dystrophin-eGFP expression 2 years after injection and to
morphological/physiological improvement. Satellite cells can also be stably
transduced and thus contribute to long-term amelioration.
Gillian Butler-Browne (Institute de Myologie-INSERM, Paris, France)
reminded us of the major problems associated with cell and/or gene therapy.
Her work aims to compare the different cell types that are currently proposed
for cell therapy. She presented the generation of immortalized human myogenic
cells that have overcome replicative aging, in collaboration with Woodring
Wright (Southwestern Medical School, Dallas, TX)
(Zhu et al., 2007). She also
discussed the impressive reconstruction results obtained in her lab from the
transplantation of human-derived AC133 cells into immunodeficient mice
(Torrente et al., 2004). The
transplanted cells show high myogenicity, can migrate almost the whole
distance of the tibialis muscle and can repopulate the satellite cell
pool.
Conclusion
Over the last 45 years, our understanding of satellite cell biology has evolved gradually. But with the advent of genetic and molecular tools, an explosion of new information has propelled the field forward during the last decade in new and unexpected ways. Without question, many of the novel results on the biology of satellite and stem cells in muscle growth and repair that were presented at this meeting, point to exciting new avenues of research that will be fruitfully explored in the coming years.
ACKNOWLEDGMENTS
We thank T. Rando, G. Cossu and J. Chamberlain for organizing the meeting, the speakers for helpful comments and V. Punch for sharing his presentation notes. We apologize to our colleagues whose work could not be discussed because of space constraints. M.R. and F.L.G. acknowledge support from NIAMS, HHMI, MDA, CIHR, the CRC Program and Jesse's Journey Foundation.
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